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Comparative pathogenesis of eosinophilic meningitis caused by Angiostrongylus mackerrasae and Angiostrongylus cantonensis in murine and guinea pig models of human infection

Published online by Cambridge University Press:  09 June 2016

MAHDIS AGHAZADEH*
Affiliation:
The University of Queensland, School of Veterinary Science, Gatton, Queensland 4343, Australia QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia
MARINA C. HARVIE
Affiliation:
QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia
HELEN C. OWEN
Affiliation:
The University of Queensland, School of Veterinary Science, Gatton, Queensland 4343, Australia
CAROLINA VERÍSSIMO
Affiliation:
Laboratório de BiologiaParasitária e Parasitologia Molecular, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil
KIERAN V. ALAND
Affiliation:
Queensland Museum and Sciencentre, Queensland 4101, Australia
SIMON A. REID
Affiliation:
The University of Queensland, School of Public Health, Herston, QLD 4006, Australia
REBECCA J. TRAUB
Affiliation:
Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, Victoria 3052, Australia
DONALD P. McMANUS
Affiliation:
QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia
JAMES S. McCARTHY
Affiliation:
QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia The University of Queensland, School of Public Health, Herston, QLD 4006, Australia
MALCOLM K. JONES
Affiliation:
The University of Queensland, School of Veterinary Science, Gatton, Queensland 4343, Australia QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia
*
*Corresponding author: Mahdis Aghazadeh, Faculty of Veterinary Science, School of Life and Environment Sciences, The University of Sydney, Camperdown, NSW 2050, Australia. Tel: +61293517083. E-mail: [email protected]

Summary

This study investigated comparatively the pathogenicity of experimental infection of mice and guinea pigs, with Angiostrongylus mackerrasae and the closely related species A. cantonensis. Time course analyses showed that A. mackerrasae causes eosinophilic meningitis in these hosts, which suggests that the species has the potential to cause meningitis in humans and domestic animals. Both A. mackerrasae and the genetically similar A. cantonensis caused eosinophilic meningitis in mice at two time points of 14 and 21 days post infection (dpi). The brain lesions in mice infected with A. mackerrasae were more granulomatous in nature and the parasites were more likely to appear degenerate compared with lesions caused by A. cantonensis. This may indicate that the mouse immune system eliminates A. mackerrasae infection more effectively. The immunologic responses of mice infected with the two Angiostrongylus species was compared by assessing ex vivo stimulated spleen derived T cells and cytokines including interferon-gamma, interleukin 4 and interleukin 17 on 14 and 21 dpi. The results were similar for mice infected with A. cantonensis and A. mackerrasae. Serum from the infected animals with either A. cantonensis or A. mackerrasae recognized total soluble antigen of A. cantonensis female worms on Western blot.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Aghazadeh, M., Reid, S. A., Aland, K. V., Restrepo, A. C., Traub, R. J., McCarthy, J. S. and Jones, M. K. (2015 a). A survey of Angiostrongylus species in definitive hosts in Queensland. International Journal for Parasitology: Parasites and Wildlife 4, 323328.Google ScholarPubMed
Aghazadeh, M., Traub, R. J., Mohandas, N., Aland, K. V., Reid, S. A., McCarthy, J. S. and Jones, M. K. (2015 b). The mitochondrial genome of Angiostrongylus mackerrasae as a basis for molecular, epidemiological and population genetic studies. Parasites and Vectors 8, 473.Google Scholar
Baums, C. G., Hermeyer, K., Leimbach, S., Adamek, M., Czerny, C. P., Horstgen-Schwark, G., Valentin-Weigand, P., Baumgartner, W. and Steinhagen, D. (2013). Establishment of a model of Streptococcus iniae meningoencephalitis in Nile tilapia (Oreochromis niloticus). Journal of Comparative Pathology 149, 94102.Google Scholar
Ben, R., Rodrigues, R., Agostini, A. A. and Graeff-Teixeira, C. (2010). Use of heterologous antigens for the immunodiagnosis of abdominal angiostrongyliasis by an enzyme-linked immunosorbent assay. Memorias do Instituto Oswaldo Cruz 105, 914917.CrossRefGoogle ScholarPubMed
Bhaibulaya, M. (1974). Experimental hybridization of Angiostrongylus mackerrasae, Bhaibulaya, 1968 and Angiostrongylus cantonensis (Chen, 1935). International Journal for Parasitology 4, 567573.CrossRefGoogle ScholarPubMed
Chan, D., Barratt, J., Roberts, T., Lee, R., Shea, M., Marriott, D., Harkness, J., Malik, R., Jones, M., Aghazadeh, M., Ellis, J. and Stark, D. (2015). The Prevalence of Angiostrongylus cantonensis/mackerrasae Complex in Molluscs from the Sydney Region. PLoS ONE 10, e0128128.Google ScholarPubMed
Collins, G. H., Rothwell, T. L., Malik, R., Church, D. B. and Dowden, M. K. (1992). Angiostrongylosis in dogs in Sydney. Australian Veterinary Journal 69, 170171.Google Scholar
Cowie, R. H. (2013). Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai'i Journal of Medicine and Public Health 72, 69.Google ScholarPubMed
Graeff-Teixeira, C., da Silva, A. C. and Yoshimura, K. (2009). Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322348.CrossRefGoogle ScholarPubMed
John, D. T. and Martinez, A. J. (1975). Animal model of human disease. Central nervous system infection with the nematode Angiostrongylus cantonenis . American Journal of Pathology 80, 345348.Google ScholarPubMed
Lindo, J. F., Escoffery, C. T., Reid, B., Codrington, G., Cunningham-Myrie, C. and Eberhard, M. L. (2004). Fatal autochthonous eosinophilic meningitis in a Jamaican child caused by Angiostrongylus cantonensis . American Journal of Tropical Medicine and Hygiene 70, 425428.CrossRefGoogle Scholar
Liu, H., Luo, X., Shen, E., Li, H., Ding, X. and Chen, D. (2013). Alteration of T cell subtypes in spleen and antibodies of serum in mice infected with Angiostrongylus cantonensis . Parasitology Research 112, 12551260.CrossRefGoogle ScholarPubMed
Mackerras, M. J. and Sandars, D. F. (1954). Lifehistory of the rat lung-worm and its migration through the brain of its host. Nature 173, 956957.Google Scholar
Mackie, J., Lacasse, C. and Spratt, D. (2013). Patent Angiostrongylus mackerrasae infection in a black flying fox (Pteropus alecto). Australian Veterinary Journal 91, 366367.Google Scholar
Mason, K. V., Prescott, C. W., Kelly, W. R. and Waddell, A. H. (1976). Letter: granulomatous encephalomyelitis of puppies due to Angiostrongylus cantonensis . Australian Veterinary Journal 52, 295.CrossRefGoogle ScholarPubMed
Morassutti, A. L., Levert, K., Perelygin, A., da Silva, A. J., Wilkins, P. and Graeff-Teixeira, C. (2012). The 31-kDa Antigen of Angiostrongylus cantonensis Comprises Distinct Antigenic Glycoproteins. Vector-Borne and Zoonotic Diseases 12, 961968.Google Scholar
Morton, N. J., Britton, P., Palasanthiran, P., Bye, A., Sugo, E., Kesson, A., Ardern-Holmes, S. and Snelling, T. L. (2013). Severe hemorrhagic Meningoencephalitis due to Angiostrongylus cantonensis among young children in Sydney, Australia. Clinical Infectious Diseases 57, 11581161.Google Scholar
Perez, O., Capron, M., Lastre, M., Venge, P., Khalife, J. and Capron, A. (1989). Angiostrongylus cantonensis: role of eosinophils in the neurotoxic syndrome (Gordon-like phenomenon). Experimental Parasitology 68, 403413.CrossRefGoogle ScholarPubMed
Sawanyawisuth, K., Takahashi, K., Hoshuyama, T., Senthong, V., Limpawattana, P., Intapan, P. M., Wilson, D., Tiamkao, S., Jitpimolmard, S. and Chotmongkol, V. (2009). Clinical factors predictive of encephalitis caused by Angiostrongylus cantonensis . American Journal of Tropical Medicine and Hygiene 81, 698701.Google Scholar
Schmid-Hempel, P. (2009). Immune defence, parasite evasion strategies and their relevance for ‘macroscopic phenomena’ such as virulence. Philosophical Transactions of the Royal Society: Biological Sciences 364, 8598.Google Scholar
Spratt, D. M. (2015). Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal of Parasitology: Parasites and Wildlife 4, 178189.Google Scholar
Sugaya, H. and Yoshimura, K. (1988). T-cell-dependent eosinophilia in the cerebrospinal fluid of the mouse infected with Angiostrongylus cantonensis . Parasite Immunology 10, 127138.CrossRefGoogle ScholarPubMed
Sugaya, H., Aoki, M., Abe, T., Ishida, K. and Yoshimura, K. (1997). Cytokine responses in mice infected with Angiostrongylus cantonensis . Parasitology Research 83, 1015.Google Scholar
Walker, A. G., Spielman, D., Malik, R., Graham, K., Ralph, E., Linton, M. and Ward, M. P. (2015). Canine neural angiostrongylosis: a case-control study in Sydney dogs. Australian Veterinary Journal 93, 195199.Google Scholar
Wang, Q. P., Lai, D. H., Zhu, X. Q., Chen, X. G. and Lun, Z. R. (2008). Human angiostrongyliasis. Lancet Infectious Diseases 8, 621630.Google Scholar
Wright, J. D., Kelly, W. R., Waddell, A. H. and Hamilton, J. (1991). Equine neural angiostrongylosis. Australian Veterinary Journal 68, 5860.CrossRefGoogle ScholarPubMed